Modulation of the host innate immune and inflammatory response by translocated bacterial proteins

Cellular Microbiology

Volumn 17, Issue 6, 2015, Pages 785-795

  Asrat, Seblewongel ^a   Davis, Kimberly M ^a   Isberg, Ralph R ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARRIER PROTEIN; CASPASE 11; CASPASE 8; F BOX PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 6; MESSENGER RNA PRECURSOR; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 3; PATTERN RECOGNITION RECEPTOR; RIBONUCLEASE H; SSPH2 PROTEIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 5; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; YERSINIA OUTER PROTEIN E; BACTERIAL SECRETION SYSTEM; VIRULENCE FACTOR;

ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; CELL DEATH; CYTOKINE PRODUCTION; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENZYME ACTIVATION; EUKARYOTIC CELL; EXTRACELLULAR SPACE; F BOX MOTIF; GENE EXPRESSION; HISTONE MODIFICATION; HOST CELL; IMMUNE RESPONSE; IMMUNOMODULATION; INFLAMMATION; INNATE IMMUNITY; LEGIONELLA; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SHIGELLA FLEXNERI; SIGNAL TRANSDUCTION; TRANSLATION INITIATION; TYPE III SECRETION SYSTEM; TYPE IV SECRETION SYSTEM; UBIQUITINATION; YERSINIA; ANIMAL; BACTERIAL SECRETION SYSTEM; BACTERIUM; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PATHOLOGY; PROTEIN TRANSPORT;

BACTERIA (MICROORGANISMS);

ANIMALS; BACTERIA; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; INFLAMMATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; VIRULENCE FACTORS;

EID: 84929998557     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12445     Document Type: Article

References (108)

1. Ashida, H., Kim, M., Schmidt-Supprian, M., Ma, A., Ogawa, M., and Sasakawa, C. (2010) A bacterial E3 ubiquitin ligase IpaH9.8 targets NEMO/IKKgamma to dampen the host NF-kappaB-mediated inflammatory response. Nat Cell Biol 12: 66-73.
2. Ashida, H., Kim, M., and Sasakawa, C. (2014) Exploitation of the host ubiquitin system by human bacterial pathogens. Nat Rev Microbiol 12: 399-413.
3. Asrat, S., Dugan, A.S., and Isberg, R.R. (2014) The frustrated host response to Legionella pneumophila is bypassed by MyD88-dependent translation of pro-inflammatory cytokines. PLoS Pathog 10: e1004229.
4. Auerbuch, V., Golenbock, D., and Isberg, R. (2009) Innate immune recognition of Yersinia pseudotuberculosis type III secretion. PLoS Pathog 5: e1000686.
5. Barry, K.C., Fontana, M.F., Portman, J.L., Dugan, A.S., and Vance, R.E. (2013) IL-1alpha signaling initiates the inflammatory response to virulent Legionella pneumophila in vivo. J Immunol 190: 6329-6339.
6. Baruch, K., Gur-Arie, L., Nadler, C., Koby, S., Yerushalmi, G., Ben-Neriah, Y., etal. (2011) Metalloprotease type III effectors that specifically cleave JNK and NF-kB. EMBO J 30: 221-231.
7. Belyi, Y., Niggeweg, R., Opitz, B., Vogelsgesang, M., Hippenstiel, S., Wilm, M., and Aktories, K. (2006) Legionella pneumophila glucosyltransferase inhibits host elongation factor 1A. Proc Natl Acad Sci USA 103: 16953-16958.
8. Bergsbaken, T., and Cookson, B. (2007) Macrophage activation redirects Yersinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis. PLoS Pathog 3: e161.
9. Bhavsar, A., Brown, N., Stoepel, J., Wiermer, M., Martin, D., Hsu, K., etal. (2013) The Salmonella type III effector SspH2 specifically exploits the NLR co-chaperone activity of SGT1 to subvert immunity. PLoS Pathog 9: e1003518.
10. Bierne, H., and Cossart, P. (2012) When bacteria target the nucleus: the emerging family of nucleomodulins. Cell Microbiol 14: 622-633.
11. Blasche, S., Mörti, M., Steuber, H., Siszler, G., Nisa, S., Schwarz, F., etal. (2013) The E. coli effector protein NleF is a caspase inhibitor. PLoS ONE 8: e58937.
12. Brandt, S., Kwok, T., Hartig, R., Konig, W., and Backert, S. (2005) NF-kappaB activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. Proc Natl Acad Sci USA 102: 9300-9305.
13. Brodsky, I., Palm, N., Sadanand, S., Ryndak, M., Sutterwala, F., Flavell, R., etal. (2010) A Yersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system. Cell Host Microbe 7: 376-387.
14. Buti, L., Spooner, E., van der Veen, A.G., Rappuoli, R., Covacci, A., and Ploegh, H.L. (2011) Helicobacter pylori cytotoxin-associated gene A (CagA) subverts the apoptosis-stimulating protein of p53 (ASPP2) tumor suppressor pathway of the host. Proc Natl Acad Sci USA 108: 9238-9243.
15. Case, C.L., Shin, S., and Roy, C.R. (2009) Asc and Ipaf inflammasomes direct distinct pathways for caspase-1 activation in response to Legionella pneumophila. Infect Immun 77: 1981-1991.
16. Case, C.L., Kohler, L.J., Lima, J.B., Strowig, T., de Zoete, M.R., Flavell, R.A., etal. (2013) Caspase-11 stimulates rapid flagellin-independent pyroptosis in response to Legionella pneumophila. Proc Natl Acad Sci USA 110: 1851-1856.
17. Casson, C.N., Copenhaver, A.M., Zwack, E.E., Nguyen, H.T., Strowig, T., Javdan, B., etal. (2013) Caspase-11 activation in response to bacterial secretion systems that access the host cytosol. PLoS Pathog 9: e1003400.
18. Chamaillard, M., Hashimoto, M., Horie, Y., Masumoto, J., and Qiu, S. (2003) An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol 4: 702-707.
19. Chaudhary, P., Eby, M., Jasmin, A., Kumar, A., Liu, L., and Hood, L. (2000) Activation of the NF-kappaB pathway by caspase 8 and its homologs. Oncogene 19: 4451-4460.
20. Chen, G.Y., and Nunez, G. (2010) Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol 10: 826-837.
21. Chung, L., Philip, N., Schmidt, V., Koller, A., Strowig, T., Flavell, R., etal. (2014) IQGAP1 is important for activation of caspase-1 in macrophages and is targeted by Yersinia pestis type III effector YopM. MBio 5: e1402-e1414.
22. Coombes, B., Coburn, B., Potter, A., Gomis, S., Mirakhur, K., Li, Y., and Finlay, B. (2005) Analysis of the contribution of Salmonella pathogenicity islands 1 and 2 to enteric disease progression using a novel bovine ileal loop model and a murine model of infectious enterocolitis. Infect Immun 73: 7161-7169.
23. Cornelis, G. (2006) The type III secretion injectisome. Nat Rev Microbiol 4: 811-825.
24. Deshaies, R.J. (1999) SCF and Cullin/Ring H2-based ubiquitin ligases. Annu Rev Cell Dev Biol 15: 435-467.
25. Dewoody, R., Merritt, P., and Marketon, M. (2013) YopK controls both rate and fidelity of Yop translocation. Mol Microbiol 87: 301-317.
26. Ensminger, A.W., and Isberg, R.R. (2010) E3 ubiquitin ligase activity and targeting of BAT3 by multiple Legionella pneumophila translocated substrates. Infect Immun 78: 3905-3919.
27. Fontana, M., and Vance, R. (2011) Two signal models in innate immunity. Immunol Rev 243: 26-39.
28. Fontana, M.F., Banga, S., Barry, K.C., Shen, X., Tan, Y., Luo, Z.Q., and Vance, R.E. (2011) Secreted bacterial effectors that inhibit host protein synthesis are critical for induction of the innate immune response to virulent Legionella pneumophila. PLoS Pathog 7: e1001289.
29. Fritz, J., Ferrero, R., Philpott, D., and Girardin, S. (2006) Nod-like proteins in immunity, inflammation and disease. Nat Immunol 7: 1250-1257.
30. Ge, J., Xu, H., Li, T., Zhou, Y., Zhang, Z., Li, S., etal. (2009) A Legionella type IV effector activates the NF-kappaB pathway by phosphorylating the IkappaB family of inhibitors. Proc Natl Acad Sci USA 106: 13725-13730.
31. Geddes, K., Rubino, S., Streutker, C., Cho, J., Magalhaes, J., Le Bourhis, L., etal. (2010) Nod1 and Nod2 regulation of inflammation in the Salmonella colitis model. Infect Immun 78: 5107-5115.
32. Girardin, S., Boneca, I., Carneiro, L., Antignac, A., and Jéhanno, M. (2003) NOD1 detects a unique muropeptide from Gram-negative bacterial peptidoglycan. Science 300: 1584-1587.
33. Hayden, M., and Ghosh, S. (2012) NF-kB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev 26: 203-234.
34. Hemrajani, C., Berger, C., Robinson, K., Marchés, O., Mousnier, A., and Frankel, G. (2010) NleH effectors interact with Bax inhibitor-1 to block apoptosis during enteropathogenic Escherichia coli infection. Proc Natl Acad Sci USA 107: 3129-3134.
35. Hicks, S.W., and Galan, J.E. (2010) Hijacking the host ubiquitin pathway: structural strategies of bacterial E3 ubiquitin ligases. Curr Opin Microbiol 13: 41-46.
36. Hsu, F., Luo, X., Qiu, J., Teng, Y.B., Jin, J., Smolka, M.B., etal. (2014) The Legionella effector SidC defines a unique family of ubiquitin ligases important for bacterial phagosomal remodeling. Proc Natl Acad Sci USA 111: 10538-10543.
37. Ivanov, S.S., and Roy, C.R. (2013) Pathogen signatures activate a ubiquitination pathway that modulates the function of the metabolic checkpoint kinase mTOR. Nat Immunol 14: 1219-1228.
38. Janeway, C., and Medzhitov, R. (2002) Innate immune recognition. Annu Rev Immunol 20: 197-216.
39. Kailasan Vanaja, S., Rathinam, V.A., Atianand, M.K., Kalantari, P., Skehan, B., Fitzgerald, K.A., and Leong, J.M. (2014) Bacterial RNA:DNA hybrids are activators of the NLRP3 inflammasome. Proc Natl Acad Sci USA 111: 7765-7770.
40. Kawai, T., and Akira, S. (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11: 373-384.
41. Kayagaki, N., Warming, S., Lamkanfi, M., Vande Walle, L., Louie, S., Dong, J., etal. (2011) Non-canonical inflammasome activation targets caspase-11. Nature 479: 117-121.
42. Kayagaki, N., Wong, M.T., Stowe, I.B., Ramani, S.R., Gonzalez, L.C., Akashi-Takamura, S., etal. (2013) Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 341: 1246-1249.
43. Kim, D., Lenzen, G., Page, A., Legrain, P., Sansonetti, P., and Parsot, C. (2005) The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc Natl Acad Sci 102: 14046-14051.
44. Klingenbeck, L., Eckart, R.A., Berens, C., and Luhrmann, A. (2013) The Coxiella burnetii type IV secretion system substrate CaeB inhibits intrinsic apoptosis at the mitochondrial level. Cell Microbiol 15: 675-687.
45. Kofoed, E.M., and Vance, R.E. (2011) Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature 477: 592-595.
46. Kubori, T., Hyakutake, A., and Nagai, H. (2008) Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions. Mol Microbiol 67: 1307-1319.
47. Kubori, T., Shinzawa, N., Kanuka, H., and Nagai, H. (2010) Legionella metaeffector exploits host proteasome to temporally regulate cognate effector. PLoS Pathog 6: e1001216.
48. Kubori, T., Koike, M., Bui, X., Higaki, S., Aizawa, S., and Nagai, H. (2014) Native structure of a type IV secretion system core complex essential for Legionella pathogenesis. Proc Natl Acad Sci 111: 11804-11809.
49. Kwuan, L., Adams, W., and Auerbuch, V. (2013) Impact of host membrane pore formation by the Yersinia pseudotuberculosis type III secretion system on the macrophage innate immune response. Infect Immun 81: 905-914.
50. Lamb, A., Yang, X.D., Tsang, Y.H., Li, J.D., Higashi, H., Hatakeyama, M., etal. (2009) Helicobacter pylori CagA activates NF-kappaB by targeting TAK1 for TRAF6-mediated Lys 63 ubiquitination. EMBO Rep 10: 1242-1249.
51. Lamkanfi, M., and Dixit, V. (2009) Inflammasomes: guardians of cytosolic sanctity. Immunol Rev 227: 95-105.
52. Lamkanfi, M., and Dixit, V.M. (2014) Mechanisms and functions of inflammasomes. Cell 157: 1013-1022.
53. LaRock, C., and Cookson, B. (2012) The Yersinia virulence effector YopM binds caspase-1 to arrest inflammasome assembly and processing. Cell Host Microbe 12: 799-805.
54. Li, S., Zhang, L., Yao, Q., Li, L., Dong, N., Rong, J., etal. (2013a) Pathogen blocks host death receptor signalling by arginine GlcNAcylation of death domains. Nature 501: 242-246.
55. Li, T., Lu, Q., Wang, G., Xu, H., Huang, H., Cai, T., etal. (2013b) SET-domain bacterial effectors target heterochromatin protein 1 to activate host rDNA transcription. EMBO Rep 14: 733-740.
56. Lomma, M., Dervins-Ravault, D., Rolando, M., Nora, T., Newton, H.J., Sansom, F.M., etal. (2010) The Legionella pneumophila F-box protein Lpp2082 (AnkB) modulates ubiquitination of the host protein parvin B and promotes intracellular replication. Cell Microbiol 12: 1272-1291.
57. Losick, V.P., Haenssler, E., Moy, M.Y., and Isberg, R.R. (2010) LnaB: a Legionella pneumophila activator of NF-kappaB. Cell Microbiol 12: 1083-1097.
58. Luhrmann, A., Nogueira, C.V., Carey, K.L., and Roy, C.R. (2010) Inhibition of pathogen-induced apoptosis by a Coxiella burnetii type IV effector protein. Proc Natl Acad Sci USA 107: 18997-19001.
59. Lutay, N., Ambite, I., Gronberg Hernandez, J., Rydstrom, G., Ragnarsdottir, B., Puthia, M., etal. (2013) Bacterial control of host gene expression through RNA polymerase II. J Clin Invest 123: 2366-2379.
60. Marenne, M., Journet, L., Mota, L., and Cornelis, G. (2003) Genetic analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: role of LcrV, YscF and YopN. Microb Pathog 35: 243-258.
61. Martinon, F., Burns, K., and Tschopp, J. (2002) The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell 10: 417-426.
62. Meinzer, U., Barreau, F., Esmiol-Welterlin, S., Jung, C., Villard, C., Léger, T., etal. (2012) Yersinia pseudotuberculosis effector YopJ subverts the Nod2/RICK/TAK1 pathway and activates caspase-1 to induce intestinal barrier dysfunction. Cell Host Microbe 11: 337-351.
63. Mejía, E., Bliska, J., and Viboud, G. (2008) Yersinia controls type III effector delivery into host cells by modulating Rho activity. PLoS Pathog 4: e3.
64. Miao, E.A., Mao, D.P., Yudkovsky, N., Bonneau, R., Lorang, C.G., Warren, S.E., etal. (2010) Innate immune detection of the type III secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci USA 107: 3076-3080.
65. Mills, E., Baruch, K., Charpentier, X., Kobi, S., and Rosenshine, I. (2008) Real-time analysis of effector translocation by the type III secretion system of enteropathogenic Escherichia coli. Cell Host Microbe 3: 104-113.
66. Mittal, R., Peak-Chew, S., and McMahon, H. (2006) Acetylation of MEK2 an I kappa B kinase (IKK) activation loop residues by YopJ inhibits signaling. Proc Natl Acad Sci 103: 18574-18579.
67. Molofsky, A.B., Byrne, B.G., Whitfield, N.N., Madigan, C.A., Fuse, E.T., Tateda, K., and Swanson, M.S. (2006) Cytosolic recognition of flagellin by mouse macrophages restricts Legionella pneumophila infection. J Exp Med 203: 1093-1104.
68. von Moltke, J., Ayres, J.S., Kofoed, E.M., Chavarria-Smith, J., and Vance, R.E. (2013) Recognition of bacteria by inflammasomes. Annu Rev Immunol 31: 73-106.
69. Mühlen, S., Ruchaud-Sparagano, M.H., and Kenny, B. (2011) Proteasome-independent degradation of canonical NFkappaB complex components by the NleC protein of pathogenic Escherichia coli. J Biol Chem 286: 5100-5107.
70. Mukherjee, S., Keitany, G., Li, Y., Wang, Y., Ball, H., Goldsmith, E., and Orth, K. (2006) Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312: 1211-1214.
71. Nadler, C., Baruch, K., Kobi, S., Mills, E., Haviv, G., Farago, M., etal. (2010) The type III secretion effector NleE inhibits NF-kappaB activation. PLoS Pathog 6: e1000743.
72. Newton, H., Pearson, J., Badea, L., Kelly, M., Lucas, M., Holloway, G., etal. (2010) The type III effectors NleE and NleB from enteropathogenic E. coli and OspZ from Shigella block nuclear translocation of NF-kappaB p65. PLoS Pathog 6: e1000898.
73. Okuda, J., Toyotome, T., Kataoka, N., Ohno, M., Abe, H., Shimura, Y., etal. (2005) Shigella effector IpaH9.8 binds to splicing factor U2AF(35) to modulate host immune responses. Biochem Biophys Res Commun 333: 531-539.
74. Orth, K., Xu, Z., Mudgett, M., Bao, Z., Palmer, L., Bliska, J., etal. (2000) Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290: 1594-1597.
75. Pallett, M., Berger, C., Pearson, J., Hartland, E., and Frankel, G. (2014) The type III secretion effector NleF of enteropathogenic Escherichia coli activates NF-kB early during infection. Infect Immun 82: 4878-4888.
76. Paquette, N., Conlon, J., Sweet, C., Rus, F., Wilson, L., Pereira, A., etal. (2012) Serine/threonine acetylation of TGFß-activated kinase (TAK1_ by Yersinia pestis YopJ inhibits innate immune signaling. Proc Natl Acad Sci 109: 12710-12715.
77. Pearson, J.S., Riedmaier, P., Marchés, O., Frankel, G., and Hartland, E.L. (2011) A type III effector protease NleC from enteropathogenic Escherichia coli targets NF-kB for degradation. Mol Microbiol 80: 219-230.
78. Pearson, J., Giogha, C., Ong, S., Kennedy, C., Kelly, M., Robinson, K., etal. (2013) A type III effector antagonizes death receptor signalling during bacterial gut infection. Nature 501: 247-251.
79. Pennini, M.E., Perrinet, S., Dautry-Varsat, A., and Subtil, A. (2010) Histone methylation by NUE, a novel nuclear effector of the intracellular pathogen Chlamydia trachomatis. PLoS Pathog 6: e1000995.
80. Price, C.T., Al-Khodor, S., Al-Quadan, T., Santic, M., Habyarimana, F., Kalia, A., and Kwaik, Y.A. (2009) Molecular mimicry by an F-box effector of Legionella pneumophila hijacks a conserved polyubiquitination machinery within macrophages and protozoa. PLoS Pathog 5: e1000704.
81. Pruneda, J., Smith, F., Daurle, A., Swaney, D., Villén, J., Scott, J., etal. (2014) E2-Ub conjugates regulate the kinase activity of Shigella effector OspG during pathogenesis. EMBO J 33: 437-449.
82. Quezada, C., Hicks, S., Galán, J., and Stebbins, C. (2009) A family of Salmonella virulence factors functions as a distinct class of autoregulated E3 ubiquitin ligases. Proc Natl Acad Sci 106: 4864-4869.
83. Ravid, T., and Hochstrasser, M. (2008) Diversity of degradation signals in the ubiquitin-proteasome system. Nat Rev Mol Cell Biol 9: 679-690.
84. Ren, T., Zamboni, D.S., Roy, C.R., Dietrich, W.F., and Vance, R.E. (2006) Flagellin-deficient Legionella mutants evade caspase-1- and Naip5-mediated macrophage immunity. PLoS Pathog 2: e18.
85. Rolando, M., Sanulli, S., Rusniok, C., Gomez-Valero, L., Bertholet, C., Sahr, T., etal. (2013) Legionella pneumophila effector RomA uniquely modifies host chromatin to repress gene expression and promote intracellular bacterial replication. Cell Host Microbe 13: 395-405.
86. Seyedarabi, A., Sullivan, J., Sasakawa, C., and Pickersgill, R. (2010) A disulfide driven domain swap switches off the activity of Shigella IpaH9.8 E3 ligase. FEBS Lett 584: 4163-4168.
87. Sham, H.P., Shames, S.R., Croxen, M.A., Ma, C., Chan, J.M., Khan, M.A., etal. (2011) Attaching and effacing bacterial effector NleC suppresses epithelial inflammatory responses by inhibiting NF-kB and p38 mitogen-activated protein kinase activation. Infect Immun 79: 3552-3562.
88. Shen, X., Banga, S., Liu, Y., Xu, L., Gao, P., Shamovsky, I., etal. (2009) Targeting eEF1A by a Legionella pneumophila effector leads to inhibition of protein synthesis and induction of host stress response. Cell Microbiol 11: 911-926.
89. Shin, S., Case, C.L., Archer, K.A., Nogueira, C.V., Kobayashi, K.S., Flavell, R.A., etal. (2008) Type IV secretion-dependent activation of host MAP kinases induces an increased proinflammatory cytokine response to Legionella pneumophila. PLoS Pathog 4: e1000220.
90. Suzuki, S., Mimuro, H., Kim, M., Ogawa, M., Ashida, H., Toyotome, T., etal. (2014) Shigella IpaH7.8 E3 ubiquitin ligase targets glomulin and activates inflammasomes to demolish macrophages. Proc Natl Acad Sci 111: E4254-E4263.
91. Sweet, C., Conlon, J., Golenbock, D., Goguen, J., and Silverman, N. (2007) YopJ targets TRAF proteins to inhibit TLR-mediated NF-kappaB, MAPK and IRF3 signal transduction. Cell Microbiol 9: 2700-2715.
92. Thiennimitr, P., Winter, S., Winter, M., Xavier, M., Tolstikov, V., Huseby, D., etal. (2011) Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci 108: 17480-17485.
93. Thorslund, S., Edgren, T., Pettersson, J., Nordfeith, R., Sellin, M., Ivanova, E., etal. (2011) The RACK1 signalling scaffold protein selectively interacts with Yersinia pseudotuberculosis virulence function. PLoS ONE 6: e16784.
94. Vallabhapurapu, S., and Karin, M. (2009) Regulation and function of NF-kappaB transcription factors in the immune system. Annu Rev Immunol 27: 693-733.
95. Vance, R., Isberg, R., and Portnoy, D. (2009) Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6: 10-21.
96. Vazquez, C.L., and Colombo, M.I. (2010) Coxiella burnetii modulates Beclin 1 and Bcl-2, preventing host cell apoptosis to generate a persistent bacterial infection. Cell Death Differ 17: 421-438.
97. Voth, D.E., Howe, D., and Heinzen, R.A. (2007) Coxiella burnetii inhibits apoptosis in human THP-1 cells and monkey primary alveolar macrophages. Infect Immun 75: 4263-4271.
98. Wan, F., Anderson, D., Barnitz, R., Snow, A., Bidere, N., Zheng, L., etal. (2007) Ribosomal protein S3: a KH domain subunit in NF-kappaB complexes that mediates selective gene regulation. Cell 131: 927-939.
99. Wan, F., Weaver, A., Gao, X., Bern, M., Hardwidge, P., and Lenardo, M. (2011) IKKß phosphorylation regulates RPS3 nuclear translocation and NF-kB function during infection with Escherichia coli strain O157:H7. Nat Immunol 12: 335-343.
100. Wang, F., Jiang, Z., Li, Y., He, X., Zhao, J., Yang, X., etal. (2013) Shigella flexneri T3SS effector IpaH4.5 modulates the host inflammatory response via interaction with NF-kB p65 protein. Cell Microbiol 15: 474-485.
101. Wei, J., Noto, J.M., Zaika, E., Romero-Gallo, J., Piazuelo, M.B., Schneider, B., etal. (2014) Bacterial CagA protein induces degradation of p53 protein in a p14ARF-dependent manner. Gut. Published Online First: July 30, 2014.
102. Winter, S., Thiennimitr, P., Winter, M., Butler, B., Huseby, D., Crawford, R., etal. (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467: 426-429.
103. Xiao, B., Wilson, J., and Gamblin, S. (2003) SET domains and histone methylation. Curr Opin Struct Biol 13: 699-705.
104. Yang, J., Zhao, Y., Shi, J., and Shao, F. (2013) Human NAIP and mouse NAIP1 recognize bacterial type III secretion needle protein for inflammasome activation. Proc Natl Acad Sci USA 110: 14408-14413.
105. Yen, H., Ooka, T., Iguchi, A., Hayashi, T., Sugimoto, N., and Tobe, T. (2010) NleC, a type III secretion protease, compromises NF-kB activation by targeting p65/RelA. PLoS Pathog 6: e1001231.
106. Zhou, H., Monack, D., Kayagaki, N., Wertz, I., Yin, J., Wolf, B., and Dixit, V. (2005) Yersinia virulence factor YopJ acts as a deubiquitinase to inhibit NF-kappa B activation. J Exp Med 202: 1327-1332.
107. Zhou, Y., Dong, N., Hu, L., and Shao, F. (2013) The Shigella type three secretion system effector OspG directly and specifically binds to host ubiquitin for activation. PLoS ONE 8: e57558.
108. Zwack, E., Snyder, A., Wynosky-Dolfi, M., Ruthel, G., Philip, N., Marketon, M., etal. (2015) Inflammasome activation in response to the Yersinia type III secretion system hyperinjection of translocon proteins YopB and YopD. MBio 6: e02095-02114.